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Genetic Structure and Population Differentiation of the Mediterranean Pioneer Spiny Broom Calicotome Villosa Across the Strait of Gibraltar

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Genetic Structure and Population Differentiation of the Mediterranean Pioneer Spiny Broom Calicotome Villosa Across the Strait of Gibraltar Genetic structure and population differentiation of the Mediterranean pioneer spiny broom Calicotome villosa across the Strait of Gibraltar JUAN ARROYO*, ABELARDO APARICIO, RAFAEL G. ALBALADEJO, JOAQUÍN MUÑOZ† and RITA BRAZA Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apartado 1095, E-41080 Sevilla, Spain The region around the Strait of Gibraltar is considered to be one of the most relevant ‘hot spots’ of biodiversity in the Mediterranean Basin due to its historical, biogeographical, and ecological features. Prominent among these is its role as a land bridge for the migration and differentiation of species during the Pleistocene, as a consequence of the lowering of sea level and climate changes associated with the Ice Ages. In the present study, we report a multilevel hierarchical investigation of the genetic diversity of Calicotome villosa, a common pioneer legume shrub, at the regional scale. The results of genetic analysis of progeny arrays are consistent with a predominantly outcrossing mating system in all the populations analysed. Geographically, a pattern of population isolation by distance was found, but the Strait accounted for only approximately 2% of the among-population genetic differentiation. Consequently, extensive historical gene flow appears to be the rule for this species in this area. According to the natural history traits of C. villosa (pollination, dispersal, and colonization ability), we hypothesize that gene flow must be strongly influenced by seed dispersal because pollen flow is very limited. Based on the history of trade and land use, cattle and human movements across the Strait must have strongly favoured seed dispersal. We review and discuss these results and compare them with those of other reported studies of genetic and phylogenetic differentiation across the Strait of Gibraltar. It is stressed that colonization ability, which depends upon seed dispersal and life form, can be a more critical factor in gene flow than pollination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 39–51. ADDITIONAL KEYWORDS: allozymes – breeding system – colonization – dispersal – gene flow – legume – Mediterranean biogeography – population genetics. INTRODUCTION of land bridges attempted to explain global patterns of biogeographical similarities (for a botanical per- In biogeography, some areas are of particular interest spective, see van Steenis, 1962) until it was super- because their geographical settings and historical seded by interpretations based on continental drift constraints are thought to strongly influence the (Raven & Axelrod, 1974). Some particular areas, such geographical ranges of species. Among these areas, as Beringia and Mesoamerica, are still considered as islands, refugia, and corridors are favourite targets appropriate places to study the effects of land bridges because of the strong limitations on species move- as corridors for historical species movements. This is ments, making it easier to interpret observed pat- hypothesized to be the most plausible explanation of terns (Hewitt, 2000; Holloway, 2003). The old theory the current range of several animal and plant species (Cavers, Navarro & Lowe, 2003; Brubaker et al., 2005; García-Moreno et al., 2006). One of these areas *Corresponding author. E-mail: [email protected] †Current address: Estación Biológica de Doñana, CSIC, is split by the Strait of Gibraltar, which separates the Sevilla, Spain. Eurasian and African plates at their westernmost extremities. This region has had a convulsive geologi- been suggested in two other pioneer shrub legumes, cal history, involving recurrent closings and openings Cytisus and Retama (Parker, 1997; Rodríguez-Riaño, of the Strait until the late Tertiary, 5.5 Mya (Duggen Ortega-Olivencia & Devesa, 1999a), the closest rela- et al., 2003). Although there was no physical connec- tives of Calicotome (Käss & Wink, 1997; Cubas, Pardo tion during the Pleistocene, the Ice Ages provoked a & Tahiri, 2002). lowering of the sea level, resulting in the land masses In the present study, we performed a multilevel being closer. It has been stressed that this complex hierarchical investigation of the genetic diversity, history, in terms of its geological, climatic, and tem- genetic identity, and mating system in populations of poral heterogeneity, has determined most of the evo- C. villosa at the regional scale of the Strait of Gibral- lution of the plant lineages in the Mediterranean tar. The aim was to compare the observed patterns (Thompson, 2005). This geological instability, together with those previously reported for other species with with Pleistocene climate changes, may have increased different ecological requirements, contrasting biologi- the role of the Strait of Gibraltar as an active land cal traits (growth form, pollination and dispersal bridge in the migration and differentiation of species mechanisms) and historical and geographical ranges (Quézel, 1978; Caujapé-Castells & Jansen, 2003). across the Strait of Gibraltar. Accordingly, we should A comprehensive biogeographical study of the be able to test the extent to which the Strait has regional flora is lacking, but studies focusing on the represented a barrier to gene flow and promoted standing components of biodiversity and the ecology genetic differentiation. Our expectation was that, in a of woody communities across the Strait are available species with poor pollen dispersal, patterns of genetic (Ojeda, Marañón & Arroyo, 2000; Ajbilou, Marañón & differentiation should be related to seed dispersal and Arroyo, 2006). For example, short-term ecological pro- establishment, both of which are directly related to cesses associated with strong human disturbance colonizing ability (DeWoody, Nason & Smith, 2004). regimes (especially from the last millennium to the Specifically, given their suitability in reflecting his- present day; Mikesell, 1960; Reille, 1977; Moore et al., torical patterns of genetic differentiation and breed- 1998) explain the diversity of the lesser shrub and ing systems (Hamrick & Godt, 1989), we used tree species observed in northern Morocco relative to allozyme variation to determine: (1) the genetic diver- that in southern Spain (Ojeda, Marañón & Arroyo, sity, genetic structure, and genetic identity of C. 1996a; Ajbilou et al., 2006). On an evolutionary time villosa at both the population and regional scales and scale, most phylogenetic and phylogeographical (2) the breeding system of the species in selected analyses undertaken of woody species (Arroyo et al., populations using a mixed-mating model approach 2004; Rodríguez-Sánchez et al., in press) have shown (Ritland, 2002) in relation to its migration ability. some genetic differentiation across the Strait of Finally, we discuss the results obtained in the light of Gibraltar, irrespective of taxonomic group, plant life the evidences gathered for other species in this same form, or reproductive traits. However, none of these region of high biogeographical significance. studies included widespread, pioneer species, whose large geographical ranges are due to their wide eco- logical niches (Morin & Chuine, 2006). Such a study MATERIAL AND METHODS would be useful to compare the effects of colonization ability on gene flow and on patterns of genetic varia- STUDY SPECIES tion at the regional scale. Calicotome Link [Cytiseae (= Genisteae), Legumino- Breeding systems and ecological requirements are sae] comprises four species of spiny brooms with reputedly associated with colonization and migration Mediterranean distributions. The monophyly of this processes (Baker & Stebbins, 1965), and species with genus and its genetic differentiation from other contrasted colonizing ability are particularly useful to genera have been demonstrated by Cubas et al. test these associations. Calicotome villosa (Poir.) Link (2002). Calicotome villosa is a circun Mediterranean is a common pioneer shrub, the geographical range component of the lowland shrub vegetation in open of which extends across both sides of the Strait of woodlands (Greuter, Burdet & Long, 1984–89). Gibraltar. This species usually grows in large, dense, Within the western Mediterranean area, the species and continuous populations in anthropogenic environ- is much more frequent in southern Spain and north- ments of intense land use (agriculture, herding). western Morocco, where it sometimes forms almost Although many ecological data are available for this monospecific shrublands. In this range, C. villosa is species (Ojeda, 1995; Ajbilou, 2001), detailed informa- associated with disturbance processes, mostly caused tion about its demography and reproductive biology by cattle browsing, and to a lesser extent by fire and remains very scarce and the breeding system of slashing. This species is very digestible by cattle C. villosa in particular remains unexplored. Partial (Anmar, López & González, 2005) and thus it occurs self-incompatibility or inbreeding depression has in open sites with low or no tree cover and extensive © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 39–51 Figure 1. Distribution areas of Calicotome villosa on both sides of the Strait of Gibraltar (shaded areas) and the locations of the 26 populations studied. cattle management (cows and goats). However, the Mejías, Arroyo & Marañón, 2007) typically restricted species is quite resilient to serious damage because of to deep, wet, and temperate gorges. On the other strong
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